Spontaneous clearance of primary acute hepatitis C virus infection correlated with high initial viral RNA level and rapid HVR1 evolution

Hepatology

Volumn 55, Issue 6, 2012, Pages 1684-1691

  Liu, Lin ^a,c   Fisher, Brian E ^a   Thomas, David L ^a,b   Cox, Andrea L ^a   Ray, Stuart C ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 28B; VIRUS RNA;

ACUTE HEPATITIS; ADULT; ALLELE; AMPLICON; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG USE; FEMALE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; MALE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMARY ACUTE HEPATITIS C; PRIORITY JOURNAL; PROSPECTIVE STUDY; UNINDEXED SEQUENCE; VIRAL CLEARANCE; VIREMIA;

ACUTE DISEASE; ADULT; EVOLUTION, MOLECULAR; FEMALE; GENOTYPE; HEPATITIS C; HUMANS; INTERLEUKINS; MALE; PROSPECTIVE STUDIES; RNA, VIRAL; VIRAL PROTEINS;

EID: 84861576186     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25575     Document Type: Article

References (51)

1. Ghany MG, Strader DB, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 2009; 49: 1335-1374.
2. Brant LJ, Ramsay ME, Balogun MA, Boxall E, Hale A, Hurrelle M, et al. Diagnosis of acute hepatitis C virus infection and estimated incidence in low- and high-risk English populations. J Viral Hepat 2008; 15: 871-877.
3. Maheshwari A, Ray S, Thuluvath PJ. Acute hepatitis C. Lancet 2008; 372: 321-332.
4. Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 2006; 45: 529-538.
5. Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005; 436: 946-952.
6. Cox AL, Mosbruger T, Lauer GM, Pardoll D, Thomas DL, Ray SC. Comprehensive analyses of CD8+ T cell responses during longitudinal study of acute human hepatitis C. Hepatology 2005; 42: 104-112.
7. Rutebemberwa A, Ray SC, Astemborski J, Levine J, Liu L, Dowd KA, et al. High-programmed death-1 levels on hepatitis C virus-specific T cells during acute infection are associated with viral persistence and require preservation of cognate antigen during chronic infection. J Immunol 2008; 181: 8215-8225.
8. Kim AY, Schulzezur WJ, Kuntzen T, Timm J, Kaufmann DE, Duncan JE, et al. Impaired hepatitis C virus-specific T cell responses and recurrent hepatitis C virus in HIV coinfection. PLoS Med 2006; 3: e492.
9. Cox AL, Mosbruger T, Mao Q, Liu Z, Wang XH, Yang HC, et al. Cellular immune selection with hepatitis C virus persistence in humans. J Exp Med 2005; 201: 1741-1752.
10. Koretz RL, Brezina M, Polito AJ, Quan S, Wilber J, Dinello R, et al. Non-A, non-B posttransfusion hepatitis: comparing C and non-C hepatitis. Hepatology 1993; 17: 361-365.
11. Aach RD, Stevens CE, Hollinger FB, Mosley JW, Peterson DA, Taylor PE, et al. Hepatitis C virus infection in post-transfusion hepatitis. N Engl J Med 1991; 325: 1325-1329.
12. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009; 461: 391-401.
13. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009; 461: 798-801.
14. Rauch A, Kutalik Z, Descombes P, Cai T, di IJ, Mueller T, et al. Genetic variation in IL28B is associated with chronic hepatitis C and treatment failure-a genome-wide association study. Gastroenterology 2010; 138: 1338-1345.
15. Balagopal A, Thomas DL, Thio CL. IL28B and the control of hepatitis C virus infection. Gastroenterology 2010; 139: 1865-1876.
16. Marcello T, Grakoui A, Barba-Spaeth G, Machlin ES, Kotenko SV, MacDonald MR, et al. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 2006; 131: 1887-1898.
17. Robek MD, Boyd BS, Chisari FV. Lambda interferon inhibits hepatitis B and C virus replication. J Virol 2005; 79: 3851-3854.
18. Muir AJ, Shiffman ML, Zaman A, Yoffe B, de la Torre A, Flamm S, et al. Phase 1b study of pegylated interferon lambda 1 with or without ribavirin in patients with chronic genotype 1 hepatitis C virus infection. Hepatology 2010; 52: 822-832.
19. McGovern BH, Nagami EH, Birch CE, Bowen MJ, Reyor LL, Chung RT, et al. Rate of sustained virologic response in relation to baseline hepatitis C virus (HCV) RNA level and rapid virologic clearance in persons with acute HCV infection. J Infect Dis 2009; 200: 877-881.
20. Lewis-Ximenez LL, Lauer GM, Schulze zur WJ, de Sousa PS, Ginuino CF, Paranhos-Baccala G, et al. Prospective follow-up of patients with acute hepatitis C virus infection in Brazil. Clin Infect Dis 2010; 50: 1222-1230.
21. Lechner F, Wong DK, Dunbar PR, Chapman R, Chung RT, Dohrenwend P, et al. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med 2000; 191: 1499-1512.
22. Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, Chisari FV. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 2001; 194: 1395-1406.
23. Wedemeyer H, He XS, Nascimbeni M, Davis AR, Greenberg HB, Hoofnagle JH, et al. Impaired effector function of hepatitis C virus-specific CD8+ T cells in chronic hepatitis C virus infection. J Immunol 2002; 169: 3447-3458.
24. Farci P, Shimoda A, Wong D, Cabezon T, De Gioannis D, Strazzera A, et al. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc Natl Acad Sci U S A 1996; 93: 15394-15399.
25. Bukh J, Thimme R, Meunier JC, Faulk K, Spangenberg HC, Chang KM, et al. Previously infected chimpanzees are not consistently protected against reinfection or persistent infection after reexposure to the identical hepatitis C virus strain. J Virol 2008; 82: 8183-8195.
26. Timpe JM, Stamataki Z, Jennings A, Hu K, Farquhar MJ, Harris HJ, et al. Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 2008; 47: 17-24.
27. Dowd KA, Netski DM, Wang XH, Cox AL, Ray SC. Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus. Gastroenterology 2009; 136: 2377-2386.
28. Pestka JM, Zeisel MB, Blaser E, Schurmann P, Bartosch B, Cosset FL, et al. Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc Natl Acad Sci U S A 2007; 104: 6025-6030.
29. von Hahn T, Yoon JC, Alter H, Rice CM, Rehermann B, Balfe P, et al. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 2007; 132: 667-678.
30. Liu L, Fisher BE, Dowd KA, Astemborski J, Cox AL, Ray SC. Acceleration of hepatitis C virus envelope evolution in humans is consistent with progressive humoral immune selection during the transition from acute to chronic infection. J Virol 2010; 84: 5067-5077.
31. Cox AL, Page K, Bruneau J, Shoukry NH, Lauer GM, Kim AY, et al. Rare birds in North America: acute hepatitis C cohorts. Gastroenterology 2009; 136: 26-31.
32. Osburn WO, Fisher BE, Dowd KA, Urban G, Liu L, Ray SC, et al. Spontaneous control of primary hepatitis C virus infection and immunity against persistent reinfection. Gastroenterology 2010; 138: 315-324.
33. Wang XH, Netski DM, Astemborski J, Mehta SH, Torbenson MS, Thomas DL, et al. Progression of fibrosis during chronic hepatitis C is associated with rapid virus evolution. J Virol 2007; 81: 6513-6522.
34. Liu Z, Netski DM, Mao Q, Laeyendecker O, Ticehurst JR, Wang XH, et al. Accurate representation of the hepatitis C virus quasispecies in 5.2-kilobase amplicons. J Clin Microbiol 2004; 42: 4223-4229.
35. Nickle DC, Jensen MA, Gottlieb GS, Shriner D, Learn GH, Rodrigo AG, et al. Consensus and ancestral state HIV vaccines. Science 2003; 299: 1515-1518.
36. Friedrich TC, Dodds EJ, Yant LJ, Vojnov L, Rudersdorf R, Cullen C, et al. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 2004; 10: 275-281.
37. Kuntzen T, Timm J, Berical A, Lewis-Ximenez LL, Jones A, Nolan B, et al. Viral sequence evolution in acute hepatitis C virus infection. J Virol 2007; 81: 11658-11668.
38. Ray SC, Fanning L, Wang XH, Netski DM, Kenny-Walsh E, Thomas DL. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J Exp Med 2005; 201: 1753-1759.
39. Honda M, Sakai A, Yamashita T, Nakamoto Y, Mizukoshi E, Sakai Y, et al. Hepatic Interferon-stimulated genes expression is associated with genetic variation in interleukin 28B and the outcome of interferon therapy for chronic hepatitis C. Gastroenterology 2010; 139: 499-509.
40. Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, et al. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005; 128: 1437-1444.
41. Sarasin-Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, Filipowicz W, et al. Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 2008; 105: 7034-7039.
42. Chattergoon MA, Levine JS, Latanich R, Osburn WO, Thomas DL, Cox AL. High plasma interleukin-18 levels mark the acute phase of hepatitis C virus infection. J Infect Dis 2011; 204: 1730-1740.
43. Beld M, Penning M, McMorrow M, Gorgels J, Van den Hoek A, Goudsmit J. Different hepatitis C virus (HCV) RNA load profiles following seroconversion among injecting drug users without correlation with HCV genotype and serum alanine aminotransferase levels. J Clin Microbiol 1998; 36: 872-877.
44. Villano SA, Vlahov D, Nelson KE, Cohn S, Thomas DL. Persistence of viremia and the importance of long-term follow-up after acute hepatitis C infection. Hepatology 1999; 29: 908-914.
45. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001; 413: 732-738.
46. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale MJr., Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008; 454: 523-527.
47. Hoebe K, Janssen E, Beutler B. The interface between innate and adaptive immunity. Nat Immunol 2004; 5: 971-974.
48. Asabe S, Wieland SF, Chattopadhyay PK, Roederer M, Engle RE, Purcell RH, et al. The size of the viral inoculum contributes to the outcome of hepatitis B virus infection. J Virol 2009; 83: 9652-9662.
49. Timm J, Lauer GM, Kavanagh DG, Sheridan I, Kim AY, Lucas M, et al. CD8 epitope escape and reversion in acute HCV infection. J Exp Med 2004; 200: 1593-1604.
50. Bartosch B, Verney G, Dreux M, Donot P, Morice Y, Penin F, et al. An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J Virol 2005; 79: 8217-8229.
51. Gorodkin J, Heyer LJ, Brunak S, Stormo GD. Displaying the information contents of structural RNA alignments: the structure logos. Comput Appl Biosci 1997; 13: 583-586.